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Coral larvae suppress the heat stress response during the onset of symbiosis thereby decreasing their odds of survival

Kitchen, Sheila A. and Jiang, Duo and Harii, Saki and Satoh, Noriyuki and Weis, Virginia M. and Shinzato, Chuya (2021) Coral larvae suppress the heat stress response during the onset of symbiosis thereby decreasing their odds of survival. Cold Spring Harbor Laboratory . https://resolver.caltech.edu/CaltechAUTHORS:20211213-515946000

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Abstract

The endosymbiosis between most corals and their photosynthetic dinoflagellate partners begins early in the host life history, when corals are larvae or juvenile polyps. The capacity of coral larvae to buffer climate-induced stress while in the process of symbiont acquisition could come with physiological trade-offs that alter larval behavior, development, settlement and survivorship. Here we examined the joint effects of thermal stress and symbiosis onset on colonization dynamics, survival, metamorphosis and host gene expression of Acropora digitifera larvae. We found that thermal stress decreased symbiont colonization of hosts by 50% and symbiont density by 98.5% over two weeks. Temperature and colonization also influenced larval survival and metamorphosis in an additive manner, where colonized larvae fared worse or prematurely metamorphosed more often than non-colonized larvae under thermal stress. Transcriptomic responses to colonization and thermal stress treatments were largely independent, while the interaction of these treatments revealed contrasting expression profiles of genes that function in the stress response, immunity, inflammation and cell cycle regulation. The combined treatment either canceled or lowered the magnitude of expression of heat-stress responsive genes in the presence of symbionts, revealing a physiological cost to acquiring symbionts at the larval stage with elevated temperatures. In addition, host immune suppression, a hallmark of symbiosis onset under ambient temperature, turned to immune activation under heat stress. Thus, by integrating the physical environment and biotic pressures that mediate pre-settlement event in corals, our results suggest that colonization may hinder larval survival and recruitment creating isolated, genetically similar populations under projected climate scenarios.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.12.10.472165DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/sra/PRJNA777284Related ItemNCBI Sequence Read Archive
https://github.com/skitchen19/coral_larval_heatStress_colonization_expressionRelated ItemCode to reproduce the analyses
ORCID:
AuthorORCID
Kitchen, Sheila A.0000-0003-4402-8139
Jiang, Duo0000-0002-7103-4502
Harii, Saki0000-0003-0440-7169
Satoh, Noriyuki0000-0002-4480-3572
Weis, Virginia M.0000-0002-1826-2848
Shinzato, Chuya0000-0001-7843-3381
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license. We would like to thank the students and support staff at Tropical Biosphere Research Center of University of Ryukyus and Okinawa Institute of Science and Technology Graduate University for assistance in coral collection and larval rearing. We thank Dr. Eiichi Shoguchi for providing symbiont cultures and Maria Khalturina for assistance with RNAseq library preparation. This study was supported by funding provided by NSF EAPSI OISE-1311087, JSPS-SP-13027, PADI Foundation Grant 11199, Sigma Xi Grants-in-Aid of Research and Integrative Biology Department at Oregon State University to SAK. Corals were sampled under the Okinawa Prefecture permit No. 25-67. Data Accessibility. Raw RNAseq reads are available on the NCBI Sequence Read Archive https://www.ncbi.nlm.nih.gov/sra/PRJNA777284. Code to reproduce the analyses is available at: https://github.com/skitchen19/coral_larval_heatStress_colonization_expression. Author Contributions. SAK and VMW designed the experiment. SAK performed the experiment with field and laboratory support provided by SH, NS, and CS. SAK performed the data analysis and bioinformatics. DJ contributed statistical analysis on the survival data. SAK, NS, CS and VMW provided funding for the project. SAK, VMW, and CS wrote the manuscript and all authors contributed edits. The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
NSFOISE-1311087
Japan Society for the Promotion of Science (JSPS)SP-13027
PADI Foundation11199
Sigma XiUNSPECIFIED
Subject Keywords:symbiosis onset, coral larvae, heat stress, cell cycle arrest, inflammation, cellular senescence
DOI:10.1101/2021.12.10.472165
Record Number:CaltechAUTHORS:20211213-515946000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211213-515946000
Official Citation:Coral larvae suppress the heat stress response during the onset of symbiosis thereby decreasing their odds of survival Sheila A Kitchen, Duo Jiang, Saki Harii, Noriyuki Satoh, Virginia M Weis, Chuya Shinzato bioRxiv 2021.12.10.472165; doi: https://doi.org/10.1101/2021.12.10.472165
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112370
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:13 Dec 2021 22:44
Last Modified:13 Dec 2021 22:44

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